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CytoJournal BioMed Central

Review Open Access

Time for evidence-based cytology
Pranab Dey*

Address: Department of Cytology, Postgraduate Institute of Medical Education and Research, Chandigarh, India
Email: Pranab Dey* - [email protected]
* Corresponding author

Published: 08 January 2007 Received: 30 October 2006

Accepted: 08 January 2007
CytoJournal 2007, 4:1 doi:10.1186/1742-6413-4-1
This article is available from: http://www.cytojournal.com/content/4/1/1
2007 Dey; licensee BioMed Central Ltd.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract
Evidence-based medicine (EBM) is a fashionable and an extremely hot topic for clinicians, patients
and the health service planners. Evidence-based cytology (EBC) is an offshoot of EBM. The EBC is
concerned with generating a reproducible, high quality and clinically relevant test result in the field
of cytology. This is a rapidly evolving area with high practical importance. EBC is based entirely on
research data. The various professional bodies on cytology design and recommend guidelines on
the basis of evidences. Once the guideline is implemented and practiced then the experiences of
the practicing cytopathologists may be used as a feed back to alter the existing guideline. The
various facets of EBC are sampling and specimen adequacy, morphological identification and
computer based expert system, integrated reporting, identification of the controversial areas and
high quality researches for evidences. It is the duty of the individuals and institutions to practice
EBC for better diagnosis and management of the patients. In this present paper, the various aspects
of EBC have been discussed.

Background ical science particularly in basic science. There are also

Evidence-based medicine (EBM) is a fashionable and an many newer technologies and diagnostic modalities in
extremely hot topic for clinicians, patients and the health hand. Therefore there is a need to integrate knowledge.
service planners. EBM is defined as "the conscientious, There is also a massive increase of health care costs and
explicit and judicious use of current best evidence in mak- overall workload. So it is necessary to make the best use of
ing decision about the care of individual patients [1]. Evi- finite financial resources. The general patients are now
dence-based cytology (EBC) is an offshoot of EBM. The more educated and have easier access to electronic media.
EBC is concerned with generating a reproducible, high So, they demand the best quality diagnostic tests in mini-
quality and clinically relevant test result in the field of mal period of time. Lastly there is increasing attention of
cytology. This is a rapidly evolving area with high practical the medico-legal problems in cytology. Practicing EBC
importance. To the best of my knowledge, till now there may have some role in these areas.
is no article on evidence based cytology in English litera-
ture. In this present paper I have discussed the various EBC practice in clinical cytology laboratory
aspects of EBC. Figure 1 highlights the overall view of EBC. There is need
of good quality evidences in the field of cytology. These
Increased demand for EBC evidences should be derived from high quality research
There is increased demand for EBC because of various rea- works. The basic data of cytology is handled by three
sons. There is massive explosion of knowledge in the med- branches of science, 1) statistics 2) epidemiology and 3)

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informatics. The team of experts should meet together based guideline is the most desirable one. This is based on
periodically to make guidelines. These guidelines may be systematic identification, critical appraisal, and synthesis
considered as the founder pillars of EBC. Based on the of evidences. Ideally, all the recommendations should be
guidelines the EBC could be practiced. supported by enough evidences and the evidences should
be analyzed before making guidelines. The most impor-
Guidelines in EBC tant or controversial questions should be dealt with great
There are various guidelines developed by different pro- attention and systematic review should be done on that
fessional bodies for practicing EBC [2-5]. The guidelines aspect. The method section of the guideline should be
may be opinion-based, consensus-based or evidence- clearly described by the guideline development group.
based. In opinion based guidelines, one or more experts The member of a guideline development team should be
publish their recommendations which may or may not be from expert in the field of particular branch of cytology,
opposed by others. In consensus-based guidelines, a clinicians, statistician, literature searcher and laboratory
group of experts meet and reach to a conclusive guideline. manager. The key to successful recommendation of guide-
This is relatively rapid, inexpensive method and there may line depends on multidisciplinarity of the guideline devel-
be potential bias in the recommendations [6,7]. Evidence- opment team.

Identify the questions

Search for evidences from

research data of cytology

Statistics Epidemiology Informatics Modify data

Best practice guidelines Audit practice

Practice of EBC

(EBC= Evidence based cytology)

Figure 1 of evidence-based cytology

Overview
Overview of evidence-based cytology.

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A guideline should always be realistic so that its imple- cells or agents diagnostic of a pathologic agent should be
mentation is possible. Evidence based guideline contains considered as adequate [3]. The specimens which are
graded recommendation which is influenced by the heavily contaminated and obscured by oral squamous
strength of evidence and clinical judgments. If a recom- cells, blood, inflammatory cells or air drying artefacts
mendation is not supported by high grade evidence, then should be labeled as unsatisfactory [3].
it should be based on consensus of the members [8].
A voided urine specimen can be collected in any conven-
Seeking evidences for evidence based cytology ient time of the day, 34 hours after the patient last voided
Booth et al [9] in a review on evidence based pathology and approximately 100300 ml of urine should be col-
described the methods of evidence seeking techniques in lected [2]. There is still no specific guidelines on the ade-
general. However, these could be applied in the field of quacy of urine sample. Papanicolaou's society of
cytology. The first essential stage in evidence-seeking proc- cytopathology practice guidelines task force believe that
ess is formulating or focusing our question/s. This will further studies should be done on adequacy of urine sam-
help us to use our search strategy on relevant database. ple [2].
Such as the question may be asked as "what will be the
best re-screening method in conventional cervical cytol- Accurate cervical sampling with the help of correct device/
ogy smear?". We can translate this question into a search s is the most important part of an adequate cervical smear
strategy in the form of key words: "re-screening" AND [18,19]. Inadequate sampling and sample transfer to the
"method" AND "cervical cytology". If we get systematic glass slides by the traditional or conventional method
review or meta-analysis in the search result, then we can probably the major cause of false negative cytology [20].
concentrate on these. The cytologic sampling of the cervix is taken by different
people with different background. When sampling is
We can start with MEDLINE data base as the primary faulty, the other part of the exercise such as examination
source followed by Cochrane Library and Health Technol- and reporting on the specimen are in vain. The medical
ogy Assessment database of the NHS Centre for reviews staff must receive appropriate training in taking cervical
and dissemination. sampling. A close monitor of sample adequacy rate for
each smear taker and regular feed back may improve the
Sampling and specimen adequacy, and EBC quality of the smear. In addition to properly collected
Sampling and specimen adequacy in cytology is an impor- sample, a relevant clinical data from history, inspection
tant aspect of EBC because the proper way of sample col- and palpation are also important.
lection has great impact on the test result. It is also
necessary to have adequate cells on the smear. There are The collection devices of cervical smear have great impact
various guidelines on the sampling and specimen ade- on adequacy of the materials [18]. A meta-analysis study
quacy by different expert committee [2-5,10,11] on respi- showed that the widely used Ayre's spatula is the least
ratory specimen, urine, thyroid, breast and cervical effective device for cervical sampling and gives a lower
smears. Table 1 highlights the necessary instructions yield of abnormal squamous cells [18]. Extended tip spat-
about the specimen collections in exfoliative cytology. ula along with cytobrush is the best combination of cervi-
The sensitivity of sputum cytology increases when the cal sampling devise for adequate smear [18].
samples are obtained over five consecutive days [14,15].
However it has been noted that three consecutive speci- The Bethesda System, 2001 (TBS) tried to develop a stand-
mens of sputum samples has reasonable sensitivity for ard framework on evaluation of specimen adequacy and
detection of malignancies [16]. In microscopy, well pre- reporting format [21]. According to TBS 2001, satisfactory
served, well stained cytologic material with numerous samples should have the presence of endocervical cells/
alveolar macrophages are essential for adequate sputum transformation zone (EC/TZ) component. There should
[12]. Greenberg et al noted that adequacy of a sputum be at least 10 well preserved endocervical or metaplastic
sample is directly proportional to the number of alveolar squamous cells singly or in groups (table 2) [21]. The
macrophages it contains [17]. Bronchial washings and assessment of the cellularity of the smears was also recon-
brushings are complementary to sputum cytology in the sidered in the meeting. The minimal squamous cellularity
diagnosis of respiratory tract lesions. The sample should was suggested as 8000 to 12000 well-visualized squamous
be obtained from clinically suspicious area by repetitive cells in conventional smears and 5000 squamous cells for
installation of 35 ml sterile balanced salt solution liquid based preparations [22]. It seems that the counting
through the bronchoscope. In general a large number of of individual cells is clearly impractical. What may be the
well preserved, optimally stained ciliated bronchial epi- rationality of the presence or absence of endocervical cells
thelial cells and macrophages are necessary to have a sat- related with sample adequacy? There are conflicting
isfactory specimen. However any specimen that contains reports on the presence of EC/TZ cells on cervical smears

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Table 1: Sampling and specimen adequacy of exfoliative and gynaecologic sample

Sample Specimen collection Adequacy Diagnostic categorization Guideline society

Sputum Early morning Well preserved, well 1. Non-diagnostic Papanicolaou's society

spontaneously produced stained cytologic material 2. Specific benign lesion guidelines, 1999 [3], [12]
sputum. Three adequate with numerous alveolar 3. Atypical cell present,
single specimens. [12] macrophages. [12] probably benign
4. Atypical suspicious for
malignancy
5. Malignancy
Bronchial wash and brush Specimen from clinically A large number of well As above Papanicolaou's society
suspicious area by preserved, optimally guidelines, 1999 [3]
repetitive installation of 3 stained ciliated bronchial
5 ml sterile balanced salt epithelial cells and
solution macrophages.
Voided urine sample Any convenient time, 34 No definite number of cells 1. Negative Papanicolaou's society
hours after the patient last mentioned. Probably a slide 2. Infectious agents: guidelines, 2003 [2]
voided. approximate 100 should contains at least 15 bacterial, fungal, viral
300 ml well visualized basal and 3. Nonspecific
intermediate cells [13] inflammatory changes:
acute inflammation, chronic
inflammation, consistent
with xanthogranulomatous
pyelonephritis
4. Cellular changes
associated with
chemotherapeutic agents
or radiation
5. Epithelial cell
abnormalities: a) atypical
urothelial cells, b) low
grade urothelial carcinoma
c) High grade urothelial
carcinoma d) squamous cell
carcinoma e)
adenocarcinoma f) other
malignancy
6. Other

and detection of squamous intraepithelial lesion (SIL) Criteria for determining adequacy of FNAC of thyroid
[23-26]. However, many retrospective longitudinal stud- lesion is not settled till now and it varies from institution
ies have demonstrated that lack of EC/TZ cells on smears to institution (table 3). Papanicolaou Society of Cytopa-
do not have increase chance to develop SIL [7,25]. There thology Task Forces on Standard of Practice has tried to
may be variable presence of endocervical cells in woman solve this issue [4] but ultimately did not specify any
who are pregnant, post menopausal or in oral contracep- numbers and groups of thyroid follicular epithelial cells
tives [28,29]. We should also remember that the identifi- for specimen adequacy. One group of investigators sug-
cation of EC/TZ cells is also subjected to inter-observer gest that an adequate sample should contain five to six
variability [30]. Nevertheless, the regular feedback on EC/ groups of well-preserved, well-visualized follicular cells
TZ cells may have value in improving overall specimen with each group contains 10 or more cells [33]. Another
quality, and awareness of development and use of more group has opinion that ten clusters of follicular cells with
sensitive collection technologies. It is expected that the at least 20 cells in each cluster are required to have ade-
changing incidence of cervical adenocarcinoma may alter quate sample [34]. Whereas other suggest that at least six
the implication of EC/TZ sampling [31]. It is also impor- groups of follicular cells should be present on at least two
tant to note that other adequacy factors such as obscuring of six aspirates of Fine needle aspiration cytology (FNAC)
blood or inflammation, and excessive cytolysis should be thyroid for considering adequate specimen [35]. The
evaluated in terms of their influence on sensitivity. Liquid Papanicolaou Society of Cytopathology Task Forces on
based preparations may markedly reduce blood, inflam- Standard of Practice admitted that the cellularity of a spec-
mation or air drying effect along with less number of EC/ imen is greatly influenced by nature of the lesion. Many
TZ cells [32]. The number of endocervical cells and cases of benign colloid goiter yield abundant colloid but
sqamous cells for adequacy in liquid based cytology are few follicular cells and should not be considered as inad-
still a questionable issue. equate.

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Table 2: Sampling and specimen adequacy of gynaecologic sample

Sample Specimen collection Adequacy Diagnostic categorization Guideline society

Cervical smear The whole cervix should Satisfactory samples should Negative for The 2001 Bethesda System
be visualized and the whole have the presence of intraepithelial lesion [22]
TZ area should be sampled. endocervical cells/ Epithelial cell
Cytobrush along with transformation zone abnormalities
extended tip spatula is the component. There should Squamous cell
best combination. (Lancet be at least 10 well Atypical squamous cells
review). preserved endocervical or of undetermined
Rotate the spatula through metaplastic squamous cells significance (ASC-US) and
more than one complete singly or in groups [22]. can not exclude HSIL
turn. Immediately transfer Low grade squamous
the cells to the slides and intra epithelial lesion (LSIL)
immediately fix the smear High grade squamous
by immersing in alcohol. intra epithelial lesion
(HSIL)
Squamous cell carcinoma
Glandular cell
Atypical glandular cells
Atypical glandular cells
favor neoplastic
Endocervical
adenocarcinoma in situ
Adenocarcinoma
Other
Endometrial cells in a
woman > 40 years of age

In September, 1996, the National Cancer Institute spon- ogy. These are PAPNET, AutoPap and AutoCyte Screen
sored a conference to provide a uniform guideline to [41-46]. However, no such system is available commer-
FNAC of breast [5]. The controversial topic of adequacy of cially for exfoliative cytology or FNAC smears.
breast FNA was discussed, but no specific comment was
made on requirement for a minimum number of ductal Human perception and interpretation are considered
cells for an adequate specimen. (Table 3). The task has highly valuable in diagnostic interpretation. However it is
been transferred to the aspirator and reporting pathologist of no doubt that human assessment of cytology smears
to judge the adequacy of the specimen. This particular and even histopathology sections are too some extent sub-
issue has evoked much controversy in past [36,37]. Many jective and have very low inter-observer's agreement and
studies have highlighted that the false negative FNAC of low K value in certain situations [47-50]. Various compu-
breast lesions have a low cellularity [36,38]. Therefore, ter based expert systems have been used for an objective
many authors feel that the sample having minimum approach in diagnosis [51-56]. Expert systems are compu-
number of cells should be reported as non-diagnostic ter programs that can perform reasoning tasks and can be
[39,40]. used for diagnostic difficulties. These systems are based on
Bayesian belief network (BBN), artificial neural net
Till now to best of my knowledge, no such guideline has (ANN) works, and logistic regression analysis [51-56].
been set for FNAC of lymph node and other organs.
Bayesian belief networks (BBN) have been used by vari-
Identify and interpret: What is the role of expert ous authors [51,52] to diagnose the cases of benign and
system? malignant lesions in FNAC of breast lesions. The ability of
The tasks of cytopathologist are two folds: at first he the BBN was satisfactory in diagnosis decision making. It
should sort out the representative cells or cells of interest was concluded that this expert system can help in consist-
and second, he should objectively assess the morphologic ent and objective diagnosis of breast lesions.
alteration of the cells. When the cytopathologist is chal-
lenged to detect occasional abnormal cells in the midst of Another group of researchers [53] investigated the poten-
large number of normal cells, computer assisted screening tial of the ANN for the discrimination of benign from
may be helpful. The three different automated screening malignant breast lesions. This neural network showed
techniques were developed in the field of cervical cytol- excellent performance for correct classification of cells.

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Table 3: Sampling and specimen adequacy of fine needle aspiration cytology sample

Sample Specimen collection Adequacy Diagnostic categorization Guideline society

Thyroid Multiple fine needle Different opinions Unsatisfactory for Papanicolaou's society
aspiration from different Five to six groups of well- interpretation, specific guidelines, 1996 [4]
sites or fine needle preserved, well-visualized reason(s)
sampling. follicular cells with each Benign thyroid nodule/
group contains 10 or more colloid nodule/nodular
cells. [33] goiter
Ten clusters of follicular Thyroiditis
cells with at least 20 cells in Cellular follicular lesion,
each cluster. [34] favor non-neoplastic
At least six groups of process
follicular cells should be Follicular neoplasm, favor
present on at least two of benign
six aspirates.[35] Follicular neoplasm, favor
malignant
Hurthle cell neoplasm
Malignant specific type if
possible
Other
Breast Average 24 pass in No consensus on number Benign NCI sponsored conference
palpable mass More than 2 of cells in a solid breast Atypical/indeterminate in Bethesda, Maryland 1996
passes in lesion difficult to lesion. Suspicious/probably [5]
stabilize or penetrate, dry Adequacy determined by malignant
tap or in suspected 1) opinion of the aspirator Malignant: specific types
carcinoma. 2) opinion of the Unsatisfactory Tumor/
pathologist. nuclear grading should be
incorporated in all breast
carcinomas whenever
possible.

The potential of back propagation neural networks in the ogists should take active participation in designing, evalu-
discrimination of benign from malignant thyroid lesions ating and modifying such systems.
were examined by Karakitsos P, et al [54]. It was con-
cluded that use of ANN may improve the diagnostic accu- Reporting
racy of FNA of the thyroid gland, especially in cases Reporting is one of the important components of genera-
classified as suspicious for malignancy. tion of a test result. Optimum content and format of the
report are necessary for appropriate communication with
The potential value of morphometry and ANN for dis- the clinicians and the patient. There are various guidelines
criminating benign from malignant nuclei and lesions of on the diagnostic entities in exfoliative and fine needle
the lower urinary tract on images of routinely processed aspiration cytology [2-5]. (table 1, 2, 3). Reporting for-
voided urine smears were investigated by Karakitsos P et mats can be in the form of check list type i,e proforma
al [55]. Application of ANN offered good classification at report or descriptive report or computer generated.
the nuclear and patient level and promised to become a Pathologist should be extremely careful about the termi-
powerful tool for everyday practice in the cytologic labo- nology or phases to express the certainty. Certain phrases
ratory. such as "suggestive of", "consistent with", "possibly" etc.
should be carefully used. Indiscriminate use of the phrase
Another group of researchers investigated the potential may generate confusion to the clinician [57].
value of morphometry and the back propagation neural
network for the discrimination of benign and malignant Integrated approach of reporting
lesions in images of routinely processed gastric smears In recent days, there is massive advancement in the field
stained by the Papanicolaou technique [56]. Their results of molecular biology and computer technology. The mas-
indicate that ANN and image morphometry may offer sive explosion of knowledge has also significant impact
useful information about the potential for malignancy in on cytologists. Along with cytomorphology of a lesion,
gastric cells. the cytologists now have the information of immunocyto-
chemistry, biochemical profiles and molecular details. So
This type of expert based system is valuable however the a pan-diagnostic approach is needed [58], which will be
professional societies of the pathologists and cytopathol- in other word a morpho-molecular approach to tissue

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diagnosis. The cytopathologist will have to combine the ences of the practicing cytopathologists may be used as a
clinical history of the disease with the cytomorphology, feed back to alter the existing guideline.
immunocytochemical findings and molecular details for
precise diagnosis. In future, such "molecular cytopatholo- Systematic review is also very important in EBC. It is usu-
gist" will play a central role in clinical decision making. ally moderately comprehensive and summarizes all rele-
vant research information. It identifies various limitations
Role of open access article in methodologies of different studies and also helps to
Open access extends benefits of easy access for the readers limit bias. Systematic review helps to enhance confidence
and wider real time dissemination of research areas in in overall result and also reduces delay between discovery
cytology for the authors-researchers. Some of the benefits and implementation of the knowledge. At the end it iden-
of open access and comparison with conventional tifies new research questions [68]. However systematic
method of publishing scientific knowledge are depicted in review may provide insufficient data. It is important to
a comic strip published previously [59]. The great benefits find out that whether a comprehensive and explicit search
of online open access journal are rapid turn around time, strategy has been used in the review or not? The quality of
real time publications and significant cost savings. The the included studies in the review is also important.
open access journal helps in free flow of scientific infor-
mation which is immensely important for diagnosis and The other aspect of the EBC is to employ computer based
management of diseases [59]. To avoid publication of expert system. This is in early stage of development. The
misguided substandard or faulty research, peer review of professional body of cytology can take part active role for
every article is strongly favored [60]. Cytojournal is a peer proper designing and application of these systems. Stand-
reviewed cytopathology journal which plays an important ard algorithm of reporting format may also help in diag-
role in publishing good quality research data in cytopa- nosis [69]. There should be large number of digital
thology in open access [61]. The research articles are acces- pictures available in internet web pages for guidance of
sible to any one from any part of the world independent diagnosis. Telepathology may also be helpful in diagnosis
of the financial budget of the readers [62]. The online of difficult cases.
nature allows interactive real time participation. The
reader can express their opinion immediately on any arti- The controversial areas of cytology should be identified
cle and this has definite positive impact on future of evi- and multi-institutional, multinational high quality
dence based cytology with wider participation. research works should be done. The result of these
researches should be available to all. Open access journals
Discussion and conclusion can play an important role for dissemination of knowl-
EBC is based entirely on evidences which should be of edge. In fact, there are many articles in Cytojournal on
good quality. There are many publications which have thyroid FNAC, Anal pap, lymph node FNAC, urine cytol-
described how to generate bias free good quality evi- ogy, liver etc which probably bears good impact to the
dences from a research work [63-65]. The good quality cytopathology society [70-74].
research studies can be produced by appropriate study
design of the work, explicit identification of the question, It is of no doubt that the use of a diagnostic test is an inter-
appropriate choice of sample population, application of vention [75] and the outcome of the cytologic test is part
ideal reference standard both to the test and control pop- of the decision making process that lead to an improved
ulation, blind comparison of method against reference outcome in clinical context. So we can say that a cytologic
and outcome, exclusion of confounding variables and test may improve the overall diagnostic process, therapeu-
introducing reproducible methodology. The ultimate fate tic strategy, and economic benefit. In fact it is an integral
of the research work is publication and there may be part of evidence-based medicine. However, it is interest-
potential bias in the publication of result because there is ing to note that evidence-based medicine appears to have
greater chance of publication of positive findings [66]. very little impact in the field of cytology. Probably it is
This also should be avoided as far as possible. now the ideal time to integrate our information in more
productive way for better diagnosis and management of
The various professional bodies on cytology design and the patients. This is the right time to practice evidence
recommend guidelines on the basis of evidences. We also based cytology.
should keep in mind that there is no guarantee that these
guidelines will be followed by the practicing cytologists List of abbreviations used
[67]. It is the responsibilities of the individuals or institu- EBM = Evidence-based medicine
tions to follow the most accepted guidelines. Once the
guideline is implemented and practiced then the experi- EBC = Evidence-based cytology

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